Element Concentrations and Histopathology of Liver and Kidney in West Greenland Ringed Seals (Pusa hispida).

Ringed seals are consumed in Greenland and are therefore included as a key biomonitoring species with the focus on pollution exposure and health effects. Ringed seals in Central West Greenland (Qeqertarsuaq) and in North West Greenland (Qaanaaq) were analyzed for metal concentrations in the liver and histological changes in the liver and kidney. The mean liver concentration of mercury in Qaanaaq was 3.73 ± 5.01 µg/g ww (range: 0.28-23.29 µg/g ww), and the mean cadmium concentration was 7.80 ± 8.95 µg/g ww (range: 0.013-38.79 µg/g ww). For Qeqertarsuaq, the liver concentration of mercury was 1.78 ± 1.70 µg/g ww (range: 0.45-8.00 µg/g ww) and the mean cadmium concentration was 11.58 ± 6.32 µg/g ww (range: 0.11-25.45 µg/g ww). Age had a positive effect on the liver concentrations of metals, while no effect was found for sex or histological changes. The prevalence of histological changes in liver tissue decreased in the following order: random pattern mononuclear cell infiltration (92.1%), portal cell infiltration (68.4%), hepatic intracellular fat (18.4%), portal fibrosis (7.9%), focal hepatic fibrosis (7.9%), bile duct hyperplasia/fibrosis (7.9%) and lipid granuloma (2.6%). For kidney tissue, the prevalence of histological changes decreased in the following order: glomerular mesangial deposits (54.1%) > glomerular basement membrane thickening (45.9%) > THD (40%) > tubular hyaline casts (14.0%) > glomerular atrophy (13.5%) > dilated tubules (13.5%) > glomerular hyper-cellularity (10.8%) > mononuclear cell infiltrations (8.1%).

Assessment of exposure to perfluorinated industrial substances and risk of immune suppression in Greenland and its global context: a mixed-methods study.

BACKGROUND: Perfluoroalkyl substances (PFASs) are ubiquitous global contaminants that do not readily biodegrade and are therefore routinely found worldwide in wildlife, humans, and the environment. There is a paucity of global assessments to understand regional and continental differences in exposure to PFASs and the associated health risks, including those for Indigenous Arctic communities who consume high trophic marine diets. We aimed to estimate the long-term exposure of dietary PFASs from consumption of polar bear and ringed seal meat and establish its association with blood serum concentrations of PFASs in Inuit in Ittoqoortoormiit (Scoresby Sound), East Greenland. We also aimed to assess the risk of immune suppression on the basis of European Food Safety Authority (EFSA) thresholds for weekly intake and blood serum concentrations of PFASs. Last, we conducted a worldwide risk assessment based on blood concentrations of PFASs emphasising Arctic exposure in a global context. METHODS: In this mixed-methods study, we conducted interviews to compare dietary exposure of PFASs in anonymous, non-pregnant, Inuit adults (aged ≥18 years) from full-time or part-time hunter families in Ittoqoortoormiit, East Greenland with ESFA toxic threshold values for tolerable weekly intake of the four most immunotoxic PFASs (∑4PFAS; perfluorooctanoic acid, perfluorononanoic acid, perfluorohexanesulfonic acid, and perfluorooctane sulfonate). Independent hospital staff from the local hospital randomly selected participants using simple randomisation using a telephone directory. Blood serum concentrations were then compared with EFSA risk categories: low (0·7-9·5 ng/mL), moderate (>9·5-17·5 ng/mL), high (>17·5-31·9 ng/mL), and severe (>31·9 ng/mL). We also reviewed the available scientific literature of ∑4PFAS concentrations in human blood to place the Inuit dataset in a broader global context. FINDINGS: Between Sept 21, and Oct 2, 2015, 22 participants were enrolled in the study, of which 12 were male and ten were female. Sex data were obtained from personal social security numbers and options were male or female. As a result of a subsistence diet high in marine mammal muscle, 322 (92%) of 350 people in the Ittoqoortoormiit cohort exceeded the established immunotoxic thresholds of ∑4PFASs set by EFSA's tolerable weekly intake of 4·4 ng/kg, and 301 (86%) were in the most severe risk category (>31·9 ng/mL) based on blood serum concentrations. This Inuit cohort had the highest non-occupational long-term exposure to PFASs worldwide despite their remote location relative to industrial sources. Using country-wide average values across global studies, we found that blood serum concentrations of PFASs in populations from European countries, North America, the Arctic, and Australia were generally higher than those in South America, Africa, and mainland Asia, with the highest concentrations found in people from USA, Canada, Greenland, Faroe Islands, Denmark, Iceland, Norway, Sweden, the UK, Spain, Poland, and Australia. These high exposure countries all fall within the EFSA moderate-risk and high-risk categories. INTERPRETATION: PFAS contamination of the environment and human populations occurs worldwide. This pollution not only poses substantial risks for immune system adverse events but also cardiovascular, cancerous, and reproductive endpoints. Data on such PFAS exposure is scarce in numerous countries. Therefore, it is important to also map out the exposure in these countries to enable a thorough global assessment of exposure and risks. FUNDING: Danish Cooperation for Environment in the Arctic.

Effects of chemical dispersants on feathers from Arctic seabirds.

Chemical dispersion is an oil spill response strategy where dispersants are sprayed onto the oil slick to enhance oil dispersion into the water. However, accidental application could expose seabirds to dispersants, thereby negatively affecting their plumage. To understand the possible impacts on seabirds, feathers from common eider (Somateria mollissima) and thick-billed murre (Uria lomvia) were exposed to different dosages of the dispersant Dasic Slickgone NS. For all exposure dosages the feathers increased in weight, and mostly for common eider. Analysing the feather microstructure, e.g., the Amalgamation Index, showed that larger damages were found on thick-billed murre than common eider. A no-sinking limit was established at 0.109 ml/m2. Relating this value to desktop simulations of potential sea-surface dosages in real-life situations, and to published accounts of response operations, showed that the limit is likely to be exceeded. Thus, our results show that chemical dispersants in realistic dosages could impact seabirds.

Immunologic, reproductive, and carcinogenic risk assessment from POP exposure in East Greenland polar bears (Ursus maritimus) during 1983-2013.

Polar bears (Ursus maritimus) are among the world's highest trophic level marine predators and as such have some of the highest tissue concentrations of organohalogen contaminants (OHCs) among Arctic biota. In this paper we present the results of a three decade (1983-2013) risk assessment of OHC exposure and effects on reproduction, immunity, and cancer (genotoxicity) in polar bears from Central East Greenland. Risk of adverse effects are evaluated using a risk quotient (RQ) approach with derivation from measured OHC concentrations in polar bear tissue and critical body residues (CBR) extrapolated for polar bears using physiologically-based pharmacokinetic modelling (PBPK). The additive RQs for all OHCs in polar bears were above the threshold for all effect categories (RQ > 1) in every year, suggesting this population has been at significant and continuous risk of contaminant-mediated effects for over three decades. RQs peaked in 1983 (RQ > 58) and again in 2013 (RQ > 50) after a period of decline. These trends follow ΣPCB levels during that time, and contributed almost all of the risk to immune, reproductive, and carcinogenic effects (71-99% of total RQ). The recent spike in RQs suggests a major shift in polar bear contaminant exposure from climate related changes in food composition and hereby the increased risk of adverse health effects. In the context of lifetime exposure ΣPCB and PFOS levels showed the interactive importance of year of birth, age, and emission history. In conclusion, the results indicate that East Greenland polar bears have been exposed to OHC levels over the period of 1983-2013 that potentially and continuously affected individual and theoretically also population health, with a peaking risk in the more recent years.

Effects of oil and oil burn residues on seabird feathers.

It is well known, that in case of oil spill, seabirds are among the groups of animals most vulnerable. Even small amounts of oil can have lethal effects by destroying the waterproofing of their plumage, leading to loss of insulation and buoyancy. In the Arctic these impacts are intensified. To protect seabirds, a rapid removal of oil is crucial and in situ burning could be an efficient method. In the present work exposure effects of oil and burn residue in different doses was studied on seabird feathers from legally hunted Common eider (Somateria mollissima) by examining changes in total weight of the feather and damages on the microstructure (Amalgamation Index) of the feathers before and after exposure. The results of the experiments indicate that burn residues from in situ burning of an oil spill have similar or larger fouling and damaging effects on seabird feathers, as compared to fresh oil.

Modeling Population-Level Consequences of Polychlorinated Biphenyl Exposure in East Greenland Polar Bears.

Polychlorinated biphenyls (PCBs) can cause endocrine disruption, cancer, immunosuppression, or reproductive failure in animals. We used an individual-based model to explore whether and how PCB-associated reproductive failure could affect the dynamics of a hypothetical polar bear (Ursus maritimus) population exposed to PCBs to the same degree as the East Greenland subpopulation. Dose-response data from experimental studies on a surrogate species, the mink (Mustela vision), were used in the absence of similar data for polar bears. Two alternative types of reproductive failure in relation to maternal sum-PCB concentrations were considered: increased abortion rate and increased cub mortality. We found that the quantitative impact of PCB-induced reproductive failure on population growth rate depended largely on the actual type of reproductive failure involved. Critical potencies of the dose-response relationship for decreasing the population growth rate were established for both modeled types of reproductive failure. Comparing the model predictions of the age-dependent trend of sum-PCBs concentrations in females with actual field measurements from East Greenland indicated that it was unlikely that PCB exposure caused a high incidence of abortions in the subpopulation. However, on the basis of this analysis, it could not be excluded that PCB exposure contributes to higher cub mortality. Our results highlight the necessity for further research on the possible influence of PCBs on polar bear reproduction regarding their physiological pathway. This includes determining the exact cause of reproductive failure, i.e., in utero exposure versus lactational exposure of offspring; the timing of offspring death; and establishing the most relevant reference metrics for the dose-response relationship.

Physiologically-based pharmacokinetic modelling of immune, reproductive and carcinogenic effects from contaminant exposure in polar bears (Ursus maritimus) across the Arctic.

Polar bears (Ursus maritimus) consume large quantities of seal blubber and other high trophic marine mammals and consequently have some of the highest tissue concentrations of organohalogen contaminants (OHCs) among Arctic biota. In the present paper we carried out a risk quotient (RQ) evaluation on OHC-exposed polar bears harvested from 1999 to 2008 and from 11 circumpolar subpopulations spanning from Alaska to Svalbard in order to evaluate the risk of OHC-mediated reproductive effects (embryotoxicity, teratogenicity), immunotoxicity and carcinogenicity (genotoxicity). This RQ evaluation was based on the Critical Body Residue (CBR) concept and a Physiologically-Based Pharmacokinetic Modelling (PBPK) approach using OHC concentrations measured in polar bear adipose or liver tissue. The range of OHC concentrations within polar bear populations were as follows for adipose, sum polychlorinated biphenyls ∑PCBs (1797-10,537 ng/g lw), sum methylsulphone-PCB ∑MeSO2-PCBs (110-672 ng/g lw), sum chlordanes ∑CHLs (765-3477 ng/g lw), α-hexachlorocyclohexane α-HCH (8.5-91.3 ng/g lw), ß-hexachlorocyclohexane ß-HCH (65.5-542 ng/g lw), sum chlorbenzenes ∑ClBzs (145-304 ng/g lw), dichlorodiphenyltrichloroethane ∑DDTs (31.5-206 ng/g lw), dieldrin (69-249 ng/g lw), polybrominated diphenyl ethers ∑PBDEs (4.6-78.4 ng/g lw). For liver, the perfluorooctanesulfonic acid (PFOS) concentrations ranged from 231-2792 ng/g ww. The total additive RQ from all OHCs ranged from 4.3 in Alaska to 28.6 in East Greenland bears for effects on reproduction, immune health and carcinogenicity, highlighting the important result that the toxic effect threshold (i.e. RQ>1) was exceeded for all polar bear populations assessed. PCBs were the main contributors for all three effect categories, contributing from 70.6% to 94.3% of the total risk and a RQ between 3.8-22.5. ∑MeSO2-PCBs were the second highest effect contributor for reproductive and immunological effects (0.17

Evaluation of the use of common sculpin (Myoxocephalus scorpius) organ histology as bioindicator for element exposure in the fjord of the mining area Maarmorilik, West Greenland.

The former Black Angel lead-zinc mine in Maarmorilik, West Greenland, is a historic example of how mining activity may result in a significant impact on the surrounding fjord system in terms of elevated concentrations of especially lead (Pb) and zinc (Zn) in seawater, sediments and surrounding biota. In order to shed light on the present contamination and possible effects in the fjord we initiated a range of studies including a pilot study on gill and liver morphology of common sculpins (Myoxocephalus scorpius) around Maarmorilik. Sculpins were caught and sampled at five different stations known to represent a gradient of Pb concentrations. Fish livers from all specimens were analyzed for relevant elements in the area: Fe, Zn, As, Cu, Se, Cd, Pb, Ag, Hg, Co and Ni. Lead, As and Hg showed significant differences among the five stations. For 20% of the sculpins, Hg concentrations were in the range of lowest observed effect dose (LOED) of 0.1-0.5 µg/g ww for toxic threshold on reproduction and subclinical endpoints. Likewise LOEDs for tissue lesions, LOEDs for biochemistry, growth, survival and reproduction were exceeded for Cd (0.42-1.8 µg/g ww) and for As (11.6 µg/g ww) in 28% and 85% of the sculpins, respectively. Similar to this, the no observed effect dose (NOED) for biochemistry was exceeded for Pb (0.32 µg/g ww) and for growth, mortality and reproduction for Zn (60-68 µg/g ww) in 33% and 24% of the sculpins, respectively. For all sculpins, females were significantly larger than males and for five of the elements (Fe, Co, Ni, Cu, Se) females had higher concentrations. The chronic lesions observed in liver (mononuclear cell infiltrates, necrosis, vacuolar hepatocytes, portal fibrosis, bile duct hyperplasia, active melanomacrophage centers) and gills (fusion and edema of secondary lamellae, laminar telangiectasis, mononuclear cell infiltrates, blebs) were similar to those in the literature studies for both wild and laboratory exposed sculpins and other fish species carrying similar or higher Hg concentrations. Ignoring sex and size, specimens with hepatic cell infiltrates had the highest concentrations of most elements, a relation that was also found for gill telangiectasis and Hg (all p < 0.05). When controlling for sex and size, the prevalence of vacuolar hepatocytes and endoparasites was significantly highest at the three most contaminated stations and similar differences were found for liver necrosis. We suggest that beside exposure to mining-related elements, other environmental factors, such as parasites, might be co-factors in the development of the observed liver and gill lesions. Therefore, sculpin liver and gill pathology are likely to be suitable health indicators when biomonitoring gradients of mining and other element related activity effects; while a larger study is required to fully evaluate the relationships.

A simple method to reduce the risk of cadmium exposure from consumption of Iceland scallops (Chlamys islandica) fished in Greenland.

This paper studied the levels and organ distribution of the toxic heavy metal cadmium in scallops from unpolluted Greenlandic waters. The scallops had an average cadmium concentration of 2.93 ± 0.94 µg/g wet weight in the total soft tissues and no concentration dependent effect was found for gender or size (both p>0.05). The kidney was the primary organ for cadmium accumulation with a mean of 226.2 ± 111.7 µg/g wet weight, and despite the small weight of the kidney, it appeared as the principal contributor of cadmium with 92% of the total cadmium body burden. The cadmium concentrations in the total soft tissues far exceeded the EU-limit of 1 µg/g wet weight for cadmium in bivalves. Based on this, selective evisceration of the cadmium-rich kidney and digestive gland during processing can be regarded as a reliable measure to be taken in order to reduce the cadmium content of scallops used for human consumption.

Levels and trends of toxaphene and chlordane-related pesticides in peregrine falcon eggs from South Greenland.

Peregrine falcon eggs were collected in South Greenland between 1986 and 2003 and analysed for 6 congeners of toxaphene and 5 chlordane-related pesticides (cis-chlordane, trans-chlordane, cis-nonachlor, trans-nonachlor and oxychlordane). Oxychlordane had the highest median concentration of 1448 ng/g lipid weight (lw) or 79 ng/g wet weight (ww) of all compounds. Of the toxaphene congeners, CHB-50 was the predominant congener, with a median concentration of 215 ng/g lw (15.5 ng/g ww). Chlordane-related concentrations were comparable with results from the USA, but lower than those from Canada and Norway. Toxaphene was considerably higher than in eggs of Norwegian peregrine falcon eggs, possibly reflecting different toxaphene usage in the areas of peregrine falcon migration. Toxaphene information in birds of prey is limited and comparisons with other species indicate differences in concentrations and organochlorine pattern. Temporal trends showed significant log-linear decreases for cis-chlordane and trans-chlordane, but no significant trends for other chlordanes or the toxaphene congeners, probably affected by the large variation between eggs, also of the same bird. Correlations between chlordanes and toxaphene in the Greenland peregrine falcon eggs might suggest similar sources of exposure.

What are the toxicological effects of mercury in Arctic biota?

This review critically evaluates the available mercury (Hg) data in Arctic marine biota and the Inuit population against toxicity threshold values. In particular marine top predators exhibit concentrations of mercury in their tissues and organs that are believed to exceed thresholds for biological effects. Species whose concentrations exceed threshold values include the polar bears (Ursus maritimus), beluga whale (Delphinapterus leucas), pilot whale (Globicephala melas), hooded seal (Cystophora cristata), a few seabird species, and landlocked Arctic char (Salvelinus alpinus). Toothed whales appear to be one of the most vulnerable groups, with high concentrations of mercury recorded in brain tissue with associated signs of neurochemical effects. Evidence of increasing concentrations in mercury in some biota in Arctic Canada and Greenland is therefore a concern with respect to ecosystem health.

Temporal monitoring of liver and kidney lesions in contaminated East Greenland polar bears (Ursus maritimus) during 1999-2010.

Organohalogen contaminants bioaccumulate to high concentrations in tissues of polar bears (Ursus maritimus). The exposure levels are in the order to be toxic to inner organs like liver and kidney. We therefore investigated the temporal development of lesions in liver (n=115) and kidney (n=122) samples from East Greenland polar bears taken over the 12 year period from 1999 to 2010. Seven liver and seven kidney lesions were observed of which six were age-related. Controlling for this, the analyses showed that hepatic steatosis and renal cell infiltrations, glomerular sclerosis and tubular hyperplasia decreased over the investigated time period (all p<0.05). Similarly, hypertrophy of hepatic Ito cells, renal glomerular capillary wall thickening and interstitial fibrosis increased over the study period (all p<0.05). Regarding contaminant, concentrations of polybrominated diphenyl ethers in adipose tissue were negatively associated with hepatic mononuclear cell infiltrations (p=0.05) and a similar trend was found for Hg (p=0.09). Hexachlorobenzene was positively associated with portal cell infiltrations and hepatic lipid granulomas, while polychlorinated biphenyls were negatively associated with the prevalence of steatosis (both p<0.05) and a similar trend was found for hexachlorocyclohexanes (p=0.08). Mercury was positively correlated with the frequencies of hypertrophic Ito cells (p=0.002) and a similar trend was found for perfluorooctanesulfonic acid (p=0.07). In renal tissue, hexachlorocyclohexanes were positively associated with medullar hyaline casts (p=0.03) and a similar trend was found for cell infiltrations (p=0.08). There was a trend of trans-nonachlor being positively associated with glomerular sclerosis (p=0.06) while dichlorodiphenyltrichloroethanes were negatively associated with tubular hyperplasia (p=0.02). These results suggest that specific liver and renal lesions have decreased or increased over time and that long-range transported organohalogen contaminants and mercury may be among the co-factors responsible for these observations. These relationships are important to take into account when biomonitoring health and pollution in wildlife species such as polar bears.

Improved reproductive success in otters (Lutra lutra), grey seals (Halichoerus grypus) and sea eagles (Haliaeetus albicilla) from Sweden in relation to concentrations of organochlorine contaminants.

We studied indices of reproductive outcome in three aquatic species in relation to organochlorine concentrations during four decades. In female otters, the frequency of signs of reproduction increased after 1990. In grey seals, pregnancy rate increased 1990-2010 and uterine obstructions ceased after 1993. The frequency of uterine tumours was highest 1980-2000. The number of sea eagle nestlings per checked nest increased 1985-2000, while the frequency of desiccated eggs decreased. Organochlorine concentrations decreased at annual rates between 3.5 and 10.2%. The estimated mean concentration (mg/kg lw) for total-PCB decreased from 70 to 8 (otters), from 110 to 15 (seals) and from 955 to 275 (eagles). The corresponding concentrations for ΣDDT decreased from 3.4 to 0.2 (otters), from 192 to 2.8 (seals) and from 865 to 65 (eagles). This study adds evidence to support the hypothesis that PCBs and DDTs have had strong negative effects on the reproduction and population levels of these species.

Skull pathology in East Greenland and Svalbard polar bears (Ursus maritimus) during 1892 to 2002 in relation to organochlorine pollution.

East Greenland and Svalbard polar bears (Ursus maritimus) are heavily polluted with long-range transported organochlorines such as PCBs (polychlorinated biphenyls). To investigate the negative health impacts, a time-trend study of skull pathology was conducted on 269 East Greenland and 241 Svalbard polar bears. The skulls were sampled during 1892-2002 and 1964-1992, respectively. Seven different pathological changes were found: adonti, displacement of teeth, caries, osseous proliferations, exostosis, tooth wear and periodontitis. Only tooth wear and periodontitis was in a prevalence that allowed statistical treatment. The most severe cases of tooth wear and periodontitis were accompanied by a substantial loss of alveolar bone structure. The prevalence of tooth wear and periodontitis increased significantly with age (p<0.001) with incisor wear being more severe than in canines, premolars and molars (p<0.001). No sex difference was found for tooth wear (p=0.22) while a significant difference between sexes was found for periodontitis (p=0.01) with males having higher prevalence than females (odds ratio of 2.5 for males:females). In East Greenland, the prevalence of tooth wear was significantly higher in polar bears collected in the pre pollution period (<1960) than in bears sampled during polluted periods (1960-1980 and 1981-2002) (p<0.001). Regarding periodontitis, the prevalence was not significantly different between pre-pollution and pollution periods (p=0.309). Polar bears from Svalbard had significantly higher prevalence of tooth wear (p<0.001) and periodontitis (p=0.02) than polar bears from East Greenland. The tooth wear and periodontitis odds ratios for Svalbard:East Greenland were 135 and 2.6, respectively. Hence, we found a clear age/sex link and geographical difference but no evidence for an association between skull pathology and exposure to organochlorines in East Greenland and Svalbard polar bears.

Do organohalogen contaminants contribute to histopathology in liver from East Greenland polar bears (Ursus maritimus)?

In East Greenland polar bears (Ursus maritimus), anthropogenic organohalogen compounds (OHCs) (e.g., polychlorinated biphenyls, dichlorodiphenyltrichloroethane, and polybrominated diphenyl ethers) contributed to renal lesions and are believed to reduce bone mineral density. Because OHCs are also hepatotoxic, we investigated liver histology of 32 subadult, 24 adult female, and 23 adult male East Greenland polar bears sampled during 1999-2002. Light microscopic changes consisted of nuclear displacement from the normal central cytoplasmic location in parenchymal cells, mononuclear cell infiltrations (mainly portally and as lipid granulomas), mild bile duct proliferation accompanied by fibrosis, and fat accumulation in hepatocytes and pluripotent Ito cells. Lipid accumulation in Ito cells and bile duct hyperplasia accompanied by portal fibrosis were correlated to age, whereas no changes were associated with either sex or season (summer vs. winter). For adult females, hepatocytic intracellular fat increased significantly with concentrations of the sum of hexachlorocyclohexanes, as was the case for lipid granulomas and hexachlorobenzene in adult males. Based on these relationships and the nature of the chronic inflammation, we suggest that these findings were caused by aging and long-term exposure to OHCs. Therefore, these changes may be used as biomarkers for OHC exposure in wildlife and humans. To our knowledge, this is the first time liver histology has been evaluated in relation to OHC concentrations in a mammalian wildlife species, and the information is important to future polar bear conservation strategies and health assessments of humans relying on OHC-contaminated food resources.